Monitoring ras interactions with the nucleotide exchange factor son of sevenless (Sos) using site-specific NMR reporter signals and intrinsic fluorescence

Journal of Biological Chemistry

Volumn 291, Issue 4, 2016, Pages 1703-1718

  Vo, Uybach ^a   Vajpai, Navratna ^a   Flavell, Liz ^a   Bobby, Romel ^a   Breeze, Alexander L ^a,c   Embrey, Kevin J ^a   Golovanov, Alexander P ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BINS; FEEDBACK; FLUORESCENCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDES;

FUNCTIONAL MUTANTS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INTERCONVERSIONS; INTRINSIC FLUORESCENCE; MONITORING SIGNALS; NUCLEOTIDE EXCHANGE; NUCLEOTIDE-EXCHANGE FACTOR; PROTEIN VARIANTS;

SYSTEMS ENGINEERING;

GUANOSINE DIPHOSPHATE; PROTEIN VARIANT; RAS PROTEIN; SOS PROTEIN; GUANOSINE TRIPHOSPHATE; HRAS PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN P21;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; WILD TYPE; CHEMISTRY; ENZYME ACTIVE SITE; FLUORESCENCE; GENETICS; HUMAN; METABOLISM;

ALLOSTERIC SITE; CATALYTIC DOMAIN; FLUORESCENCE; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS P21(RAS); SON OF SEVENLESS PROTEIN, DROSOPHILA;

EID: 84959020703     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.691238     Document Type: Article

References (44)

1. Pylayeva-Gupta, Y., Grabocka, E., and Bar-Sagi, D. (2011) RAS oncogenes: Weaving a tumorigenic web. Nat. Rev. Cancer 11, 761-774
2. Bourne, H. R., Sanders, D. A., and McCormick, F. (1990) The GTPase superfamily: A conserved switch for diverse cell functions. Nature 348, 125-132
3. Buday, L., and Downward, J. (2008) Many faces of Ras activation. Biochim. Biophys. Acta 1786, 178-187
4. Downward, J. (2003) Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22
5. Karapetis, C. S., Khambata-Ford, S., Jonker, D. J., O'Callaghan, C. J., Tu, D., Tebbutt, N. C., Simes, R. J., Chalchal, H., Shapiro, J. D., Robitaille, S., Price, T. J., Shepherd, L., Au, H. J., Langer, C., Moore, M. J., and Zalcberg, J. R. (2008) K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N. Engl. J. Med. 359, 1757-1765
6. Tan, C., and Du, X. (2012) KRAS mutation testing in metastatic colorectal cancer. World J. Gastroenterol. 18, 5171-5180
7. Cox, A. D., Fesik, S. W., Kimmelman, A. C., Luo, J., and Der, C. J. (2014) Drugging the undruggable RAS: Mission possible? Nat. Rev. Drug Discov. 13, 828-851
8. Boriack-Sjodin, P. A., Margarit, S. M., Bar-Sagi, D., and Kuriyan, J. (1998) The structural basis of the activation of Ras by Sos. Nature 394, 337-343
9. Rojas, J. M., Oliva, J. L., and Santos, E. (2011) Mammalian son of sevenless guanine nucleotide exchange factors: Old concepts and new perspectives. Genes Cancer 2, 298-305
10. Margarit, S. M., Sondermann, H., Hall, B. E., Nagar, B., Hoelz, A., Pirruccello, M., Bar-Sagi, D., and Kuriyan, J. (2003) Structural evidence for feedback activation by Ras-GTP of the Ras-specific nucleotide exchange factor SOS. Cell 112, 685-695
11. Sondermann, H., Soisson, S. M., Boykevisch, S., Yang, S. S., Bar-Sagi, D., and Kuriyan, J. (2004) Structural analysis of autoinhibition in the Ras activator son of sevenless. Cell 119, 393-405
12. Freedman, T. S., Sondermann, H., Friedland, G. D., Kortemme, T., Bar-Sagi, D., Marqusee, S., and Kuriyan, J. (2006) A Ras-induced conformational switch in the Ras activator son of sevenless. Proc. Natl. Acad. Sci. U.S.A. 103, 16692-16697
13. Iversen, L., Tu, H.-L., Lin, W.-C., Christensen, S. M., Abel, S. M., Iwig, J., Wu, H.-J., Gureasko, J., Rhodes, C., Petit, R. S., Hansen, S. D., Thill, P., Yu, C.-H., Stamou, D., Chakraborty, A. K., Kuriyan, J., and Groves, J. T. (2014) Ras activation by SOS: Allosteric regulation by altered fluctuation dynamics. Science 345, 50-54
14. Gureasko, J., Galush, W. J., Boykevisch, S., Sondermann, H., Bar-Sagi, D., Groves, J. T., and Kuriyan, J. (2008) Membrane-dependent signal integra-tion by the Ras activator son of sevenless. Nat. Struct. Mol. Biol. 15, 452-461
15. Lenzen, C., Cool, R. H., Prinz, H., Kuhlmann, J., and Wittinghofer, A. (1998) Kinetic analysis by fluorescence of the interaction between Ras and the catalytic domain of the guanine nucleotide exchange factor Cdc25Mm. Biochemistry 37, 7420-7430
16. Mazhab-Jafari, M. T., Marshall, C. B., Smith, M., Gasmi-Seabrook, G. M., Stambolic, V., Rottapel, R., Neel, B. G., and Ikura, M. (2010) Real-time NMR study of three small GTPases reveals that fluorescent 2-(3-)-O-(Nmethylanthraniloyl)-tagged nucleotides alter hydrolysis and exchange kinetics. J. Biol. Chem. 285, 5132-5136
17. Smith, M. J., Neel, B. G., and Ikura, M. (2013) NMR-based functional profiling of RASopathies and oncogenic RAS mutations. Proc. Natl. Acad. Sci. U.S.A. 110, 4574-4579
18. Shah, B. H., and Catt, K. J. (2004) GPCR-mediated transactivation of RTKs in the CNS: Mechanisms and consequences. Trends Neurosci. 27, 48-53
19. Bondeva, T., Balla, A., Várnai, P., and Balla, T. (2002) Structural determinants of Ras-Raf interaction analyzed in live cells. Mol. Biol. Cell 13, 2323-2333
20. Williams, J. G., Drugan, J. K., Yi, G. S., Clark, G. J., Der, C. J., and Campbell, S. L. (2000) Elucidation of binding determinants and functional consequences of Ras/Raf-cysteine-rich domain interactions. J. Biol. Chem. 275, 22172-22179
21. Spoerner, M., Herrmann, C., Vetter, I. R., Kalbitzer, H. R., and Wittinghofer, A. (2001) Dynamic properties of the Ras switch I region and its importance for binding to effectors. Proc. Natl. Acad. Sci. U.S.A. 98, 4944-4949
22. Spoerner, M., Hozsa, C., Poetzl, J. A., Reiss, K., Ganser, P., Geyer, M., and Kalbitzer, H. R. (2010) Conformational states of human rat sarcoma (Ras) protein complexed with its natural ligand GTP and their role for effector interaction and GTP hydrolysis. J. Biol. Chem. 285, 39768-39778
23. Ito, Y., Yamasaki, K., Iwahara, J., Terada, T., Kamiya, A., Shirouzu, M., Muto, Y., Kawai, G., Yokoyama, S., Laue, E. D., Wälchli, M., Shibata, T., Nishimura, S., and Miyazawa, T. (1997) Regional polysterism in the GTPbound form of the human c-Ha-Ras protein. Biochemistry 36, 9109-9119
24. Araki, M., Shima, F., Yoshikawa, Y., Muraoka, S., Ijiri, Y., Nagahara, Y., Shirono, T., Kataoka, T., and Tamura, A. (2011) Solution structure of the state 1 conformer of GTP-bound H-Ras protein and distinct dynamic properties between the state 1 and state 2 conformers. J. Biol. Chem. 286, 39644-39653
25. Spoerner, M., Nuehs, A., Herrmann, C., Steiner, G., and Kalbitzer, H. R. (2007) Slow conformational dynamics of the guanine nucleotide-binding protein Ras complexed with the GTP analogue GTP-S. FEBS J. 274, 1419-1433
26. Sprangers, R., and Kay, L. E. (2007) Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445, 618-622
27. Vo, U., Embrey, K. J., Breeze, A. L., and Golovanov, A. P. (2013) 1H, 13Cand 15N resonance assignment for the human K-Ras at physiological pH. Biomol. NMR Assign. 7, 215-219
28. Golovanov, A. P., Hautbergue, G. M., Wilson, S. A., and Lian, L. Y. (2004) A simple method for improving protein solubility and long-term stability. J. Am. Chem. Soc. 126, 8933-8939
29. Johnson, B. A., and Blevins, R. A. (1994) NMR View: A computer program for the visualization and analysis ofNMRdata. J. Biomol.NMR4, 603-614
30. Leatherbarrow, R. J. (1992) GraFit, Version 3.0. Data Analysis and Graphics program for the IBM PC, Erithacus Software, Surrey, UK
31. Mou, T. C., Gille, A., Fancy, D. A., Seifert, R., and Sprang, S. R. (2005) Structural basis for the inhibition of mammalian membrane adenylyl cyclase by 2-(3-)-O-(N-methylanthraniloyl)-guanosine 5-triphosphate. J. Biol. Chem. 280, 7253-7261
32. Gureasko, J., Kuchment, O., Makino, D. L., Sondermann, H., Bar-Sagi, D., and Kuriyan, J. (2010) Role of the histone domain in the autoinhibition and activation of the Ras activator Son of Sevenless. Proc. Natl. Acad. Sci. U.S.A. 107, 3430-3435
33. Sondermann, H., Nagar, B., Bar-Sagi, D., and Kuriyan, J. (2005) Computational docking and solution x-ray scattering predict a membrane-interacting role for the histone domain of the Ras activator son of sevenless. Proc. Natl. Acad. Sci. U.S.A. 102, 16632-16637
34. Stoffregen, M. C., Schwer, M. M., Renschler, F. A., and Wiesner, S. (2012) Methionine scanning as an NMR tool for detecting and analyzing biomolecular interaction surfaces. Structure 20, 573-581
35. Kovrigin, E. L. (2012) NMR line shapes and multi-state binding equilibria. J. Biomol. NMR 53, 257-270
36. Mas, G., Crublet, E., Hamelin, O., Gans, P., and Boisbouvier, J. (2013) Specific labeling and assignment strategies of valine methyl groups for NMR studies of high molecular weight proteins. J. Biomol. NMR 57, 251-262
37. Gelis, I., Bonvin, A. M., Keramisanou, D., Koukaki, M., Gouridis, G., Karamanou, S., Economou, A., and Kalodimos, C. G. (2007) Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131, 756-769
38. Krishnarjuna, B., Jaipuria, G., Thakur, A., D'Silva, P., and Atreya, H. S. (2011) Amino acid selective unlabeling for sequence specific resonance assignments in proteins. J. Biomol. NMR 49, 39-51
39. Quinlan, M. P., Quatela, S. E., Philips, M. R., and Settleman, J. (2008) Activated Kras, but not Hras or Nras, may initiate tumors of endodermal origin via stem cell expansion. Mol. Cell. Biol. 28, 2659-2674
40. Ford, B., Skowronek, K., Boykevisch, S., Bar-Sagi, D., and Nassar, N. (2005) Structure of the G60A mutant of Ras: Implications for the dominant negative effect. J. Biol. Chem. 280, 25697-25705
41. Kunzelmann, S., and Webb, M. R. (2011) Fluorescence detection of GDP in real time with the reagentless biosensor rhodamine-ParM. Biochem. J. 440, 43-49
42. Burns, M. C., Sun, Q., Daniels, R. N., Camper, D., Kennedy, J. P., Phan, J., Olejniczak, E. T., Lee, T., Waterson, A. G., Rossanese, O. W., and Fesik, S. W. (2014) Approach for targeting Ras with small molecules that activate SOS-mediated nucleotide exchange. Proc. Natl. Acad. Sci. U.S.A. 111, 3401-3406
43. Hall, B. E., Yang, S. S., Boriack-Sjodin, P. A., Kuriyan, J., and Bar-Sagi, D. (2001) Structure-based mutagenesis reveals distinct functions for Ras switch 1 and switch 2 in Sos-catalyzed guanine nucleotide exchange. J. Biol. Chem. 276, 27629-27637
44. Winter, J. J., Anderson, M., Blades, K., Brassington, C., Breeze, A. L., Chresta, C., Embrey, K., Fairley, G., Faulder, P., Finlay, M. R., Kettle, J. G., Nowak, T., Overman, R., Patel, S. J., Perkins, P., Spadola, L., Tart, J., Tucker, J. A., and Wrigley, G. (2015) Small molecule binding sites on the Ras:Sos complex can be exploited for inhibition of Ras activation. J. Med. Chem. 58, 2265-2274